Abstract
The composition of plant–pollinator interactions—i.e., who interacts with whom in diverse communities—is highly dynamic, and we have a very limited understanding of how interaction identities change in response to perturbations in nature. One prediction from niche and diet theory is that resource niches will broaden to compensate for resource reductions driven by perturbations, yet this has not been empirically tested in plant–pollinator systems in response to real-world perturbations in the field. Here, we use a long-term dataset of floral visitation to Ipomopsis aggregata, a montane perennial herb, to test whether the breadth of its floral visitation niche (i.e., flower visitor richness) changed in response to naturally occurring drought perturbations. Fewer floral resources are available in drought years, which could drive pollinators to expand their foraging niches, thereby expanding plants’ floral visitation niches. We compared two drought years to three non-drought years to analyze changes in niche breadth and community composition of floral visitors to I. aggregata, predicting broadened niche breadth and distinct visitor community composition in drought years compared to non-drought years. We found statistically significant increases in niche breadth in drought years as compared to non-drought conditions, but no statistically distinguishable changes in community composition of flower visitors. Our findings suggest that plants’ floral visitation niches may exhibit considerable plasticity in response to disturbance. This may have widespread consequences for community-level stability as well as functional consequences if increased niche overlap affects pollination services.
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References
Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant–pollinator interaction network. Oikos 117:1796–1807
Arroyo MT, Robles V, Tamburrino Í, Martínez-Harms J, Garreaud RD, Jara-Arancio P, Pliscoff P, Copier A, Arenas J, Keymer J (2020) Extreme drought affects visitation and seed set in a plant species in the Central Chilean Andes heavily dependent on hummingbird pollination. Plants 9:1553. https://doi.org/10.3390/plants9111553
Baskett CA, Emery SM, Rudgers JA (2011) Pollinator visits to threatened species are restored following invasive plant removal. Int J Plant Sci 172:411–422. https://doi.org/10.1086/658182
Bigger DS, Fox LR (1997) High-density populations of diamondback moth have broader host-plant diets. Oecologia 112:179–186
Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. https://doi.org/10.1086/343878
Bolnick DI, Ingram T, Stutz WE, Snowberg LK, Lau OL, Paull JS (2010) Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc R Soc Lond B Biol Sci 277:1789–1797
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Machler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400
Brosi BJ (2016) Pollinator specialization: from the individual to the community. New Phytol 210:1190–1194
Brosi B, Briggs H (2013) Single pollinator species losses reduce floral fidelity and plant reproductive function. Proc Natl Acad Sci USA 110:13044–13048. https://doi.org/10.1073/pnas.1307438110
Brosi BJ, Niezgoda K, Briggs HM (2017) Experimental species removals impact the architecture of pollination networks. Biol Lett 13:20170243. https://doi.org/10.1098/rsbl.2017.0243
Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139
Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615. https://doi.org/10.1126/science.1232728
Campbell DR (2019) Early snowmelt projected to cause population decline in a subalpine plant. Proc Natl Acad Sci 116:12901–12906. https://doi.org/10.1073/pnas.1820096116
Campbell DR, Dooley JL (1992) The spatial scale of genetic differentiation in a hummingbird-pollinated plant: comparison with models of isolation by distance. Am Nat 139:735–748
Campbell DR, Motten AF (1985) The Mechanism of competition for pollination between two forest herbs. Ecology 66:554–563. https://doi.org/10.2307/1940404
Campbell DR, Waser NM (2007) Evolutionary dynamics of an Ipomopsis hybrid zone: confronting models with lifetime fitness data. Am Nat 169:298–310. https://doi.org/10.1086/510758
CaraDonna PJ, Waser NM (2020) Temporal flexibility in the structure of plant–pollinator interaction networks. Oikos. https://doi.org/10.1111/oik.07526
CaraDonna PJ, Iler AM, Inouye DW (2014) Shifts in flowering phenology reshape a subalpine plant community. Proc Natl Acad Sci 111:4916–4921. https://doi.org/10.1073/pnas.1323073111
CaraDonna PJ, Petry WK, Brennan RM, Cunningham JL, Bronstein JL, Waser NM, Sanders NJ (2017) Interaction rewiring and the rapid turnover of plant–pollinator networks. Ecol Lett 20:385–394
Chao A, Chazdon RL, Colwell RK, Shen T-J (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:361–371
Chazdon R, Colwell R, Denslow J, Guariguata M (1998) Statistical methods for estimating species richness of woody regeneration in primary and secondary rain forests of NE Costa Rica. In: Dallmeier F, Comiskey JA (eds) In Forest biodiversity research, monitoring and modelling, pp 285–309
Chittka L, Thomson JD (1997) Sensori-motor learning and its relevance for task specialization in bumble bees. Behav Ecol Sociobiol 41:385–398. https://doi.org/10.1007/s002650050400
Cresswell JE (1999) The influence of nectar and pollen availability on pollen transfer by individual flowers of oil-seed rape (Brassica napus) when pollinated by bumblebees (Bombus lapidarius). J Ecol 87:670–677. https://doi.org/10.1046/j.1365-2745.1999.00385.x
Delignette-Muller ML, Dutang C (2015) fitdistrplus: an R package for fitting distributions. J Stat Softw 64:1–34
Emlen JM (1966) The role of time and energy in food preference. Am Nat 100:611–617
Fontaine C, Collin CL, Dajoz I (2008) Generalist foraging of pollinators: diet expansion at high density. J Ecol 96:1002–1010
Forrest JRK, Cross R, CaraDonna PJ (2019) Two-year bee, or not two-year bee? How voltinism is affected by temperature and season length in a high-elevation solitary bee. Am Nat 193:560–574
Fründ J, Dormann CF, Holzschuh A, Tscharntke T (2013) Bee diversity effects on pollination depend on functional complementarity and niche shifts. Ecology 94:2042–2054. https://doi.org/10.1890/12-1620.1
Galen C, Gregory T (1989) Interspecific pollen transfer as a mechanism of competition: Consequences of foreign pollen contamination for seed set in the alpine wildflower, Polemonium viscosum. Oecologia 81:120–123. https://doi.org/10.1007/bf00377020
Gegear RJ, Laverty TM (1995) Effect of flower complexity on relearning flower-handling skills in bumble bees. Can J Zool 73:2052–2058. https://doi.org/10.1139/z95-241
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596
Hallett AC, Mitchell RJ, Chamberlain ER, Karron JD (2017) Pollination success following loss of a frequent pollinator: the role of compensatory visitation by other effective pollinators. AoB PLANTS. https://doi.org/10.1093/aobpla/plx020
Hartig F (2019) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.2.4
Horn HS (1966) Measurement of “overlap” in comparative ecological studies. Am Nat 100:419–424
Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456. https://doi.org/10.1111/2041-210X.12613
Inouye DW (1978) Resource partitioning in bumblebees: experimental studies of foraging behavior. Ecology 59:672–678
Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362
Inouye DW, McGuire AD (1991) Effects of snowpack on timing and abundance of flowering in Delphinium nelsonii (Ranunculaceae): implications for climate change. Am J Bot 78:997–1001
Juenger T, Bergelson J (2000) Factors limiting rosette recruitment in scarlet gilia, Ipomopsis aggregata: seed and disturbance limitation. Oecologia 123:358–363
Klein A-M, Cunningham SA, Bos M, Steffan-Dewenter I (2008) Advances in pollination ecology from tropical plantation crops. Ecology 89:935–943
Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L (2005) Pollen limitation of plant reproduction: pattern and process. Annu Rev Ecol Evol Syst 36:467–497. https://doi.org/10.1146/annurev.ecolsys.36.102403.115320
Koski MH, Ison JL, Padilla A, Pham AQ, Galloway LF (2018) Linking pollinator efficiency to patterns of pollen limitation: small bees exploit the plant–pollinator mutualism. Proc R Soc B Biol Sci 285:20180635
Laverty TM (1994) Bumble bee learning and flower morphology. Anim Behav 47:531–545. https://doi.org/10.1006/anbe.1994.1077
Levine MT, Paige KN (2004) Direct and indirect effects of drought on compensation following herbivory in scarlet gilia. Ecology 85:3185–3191
MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609
Maldonado MB, Lomáscolo SB, Vázquez DP (2013) The importance of pollinator generalization and abundance for the reproductive success of a generalist plant. PLoS ONE 8:e75482. https://doi.org/10.1371/journal.pone.0075482
Mayfield MM, Waser NM, Price MV (2001) Exploring the ‘most effective pollinator principle’ with complex flowers: bumblebees and Ipomopsis aggregata. Ann Bot 88:591–596. https://doi.org/10.1006/anbo.2001.1500
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc Lond B Biol Sci 271:2605–2611
Morales CL, Traveset A (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Crit Rev Plant Sci 27:221–238. https://doi.org/10.1080/07352680802205631
Morse DH (1977) Resource partitioning in bumble bees: the role of behavioral factors. Science 197:678–680
Neff JL, Simpson BB (1990) The roles of phenology and reward structure in the pollination biology of wild sunflower (Helianthus annuus L. Asteraceae). Isr J Plant Sci 39:197–216. https://doi.org/10.1080/0021213X.1990.10677144
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, Ohara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Package ‘vegan.’ Commun Ecol Package Version 2:1–295
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326
Phillips BB, Shaw RF, Holland MJ, Fry EL, Bardgett RD, Bullock JM, Osborne JL (2018) Drought reduces floral resources for pollinators. Glob Change Biol 24:3226–3235. https://doi.org/10.1111/gcb.14130
Price MV, Waser NM, Irwin RE, Campbell DR, Brody AK (2005) Temporal and spatial variation in pollination of a montane herb: a seven-year study. Ecology 86:2106–2116. https://doi.org/10.1890/04-1274
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rathcke BJ (2000) Hurricane causes resource and pollination limitation of fruit set in a bird-pollinated shrub. Ecology 81:1951–1958. https://doi.org/10.1890/0012-9658(2000)081[1951:HCRAPL]2.0.CO;2
Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369–404
Svanbäck R, Bolnick DI (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proc R Soc Lond B Biol Sci 274:839–844. https://doi.org/10.1098/rspb.2006.0198
Thomson DM (2016) Local bumble bee decline linked to recovery of honey bees, drought effects on floral resources. Ecol Lett 19:1247–1255. https://doi.org/10.1111/ele.12659
Vanbergen AJ, Woodcock BA, Gray A, Grant F, Telford A, Lambdon P, Chapman DS, Pywell RF, Heard MS, Cavers S (2014) Grazing alters insect visitation networks and plant mating systems. Funct Ecol 28:178–189. https://doi.org/10.1111/1365-2435.12191
Vázquez DP, Simberloff D (2002) Ecological specialization and susceptibility to disturbance: conjectures and refutations. Am Nat 159:606–623. https://doi.org/10.1086/339991
Vázquez DP, Morris WF, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett 8:1088–1094. https://doi.org/10.1111/j.1461-0248.2005.00810.x
Vieira MC, Almeida-Neto M (2015) A simple stochastic model for complex coextinctions in mutualistic networks: robustness decreases with connectance. Ecol Lett 18:144–152
Waser NM (1978) Competition for hummingbird pollination and sequential flowering in two Colorado wildflowers. Ecology 59:934–944. https://doi.org/10.2307/1938545
Waser NM, Fugate ML (1986) Pollen precedence and stigma closure: a mechanism of competition for pollination between Delphinium nelsonii and Ipomopsis aggregata. Oecologia 70:573–577. https://doi.org/10.1007/bf00379906
Waser NM, Price MV (2016) Drought, pollen and nectar availability, and pollination success. Ecology 97:1400–1409. https://doi.org/10.1890/15-1423.1
Waser N, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060. https://doi.org/10.2307/2265575
Waser NM, CaraDonna PJ, Price MV (2018) Atypical flowers can be as profitable as typical hummingbird flowers. Am Nat 192:644–653
Weinstein BG, Graham CH (2017) Persistent bill and corolla matching despite shifting temporal resources in tropical hummingbird–plant interactions. Ecol Lett 20:326–335
Woodward GL, Laverty TM (1992) Recall of flower handling skills by bumble bees: a test of Darwin’s interference hypothesis. Anim Behav 44:1045–1051. https://doi.org/10.1016/S0003-3472(05)80316-1
Acknowledgements
M. Price, A. Brody, D. Campbell, R. Irwin, and N. Waser contributed data that were critical to the success of this project. We thank A. Curtsdotter, T. Reynolds, A. Fife, and D. MacArthur-Waltz for field assistance in 2018. M. Sharer led field data collection in 2019 before sampling was abandoned. In 2012, we had assistance from L. Anderson, K. Niezgoda, A. Petroff, and N. Vila-Santana. In previous years we acknowledge P. Aigner, R. Bollier, X. Colleau, P. Flanagan, C. Engel, D. Graydon, B. Koch, C. Koehler, D. Massart, H. Mayer, M. Mayfield, B. Peterson, H. Prendeville, A. Price, J. Ruvinsky, K. Sharaf, N. Thorne, G. Pederson, A. Valdenaire, and E. Wilkinson for their work in field data collection. Special thanks to the Rocky Mountain Biological Laboratory for space and research support during fieldwork. Permission to work on US Forest Service land provided through the Rocky Mountain Biological Laboratory Special Use Permit.
Funding
Field collection support for this project was provided by the National Science Foundation (DEB-1120572 and DEB-1834497 to BJB); a Lester Research Grant through the Emory University Department of Environmental Sciences (to KLE); and the ARCS Foundation (to CNM).
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KLE and CNM contributed equally to this paper. HMB conceptualized the study. KLE, CNM, XL, and BB analyzed the data. KLE, CNM, and BB drafted the manuscript. All authors contributed to data collection. All authors contributed critically to editing the manuscript and gave final approval for publication.
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Communicated by Moshe Inbar.
Understanding how species change interaction partners following disturbance is key for managing ecosystems impacted by ongoing environmental change. This work supports the hypothesis—driven by diet theory—that the set of flower visitor interaction partners would increase to a focal plant in lower-resource (drought) conditions. This work is novel in its use of a predictive theoretical framework, its leveraging of long-term data on flower visitation, and its analytical framework that allows cohesive comparison of disparately collected data.
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Endres, K.L., Morozumi, C.N., Loy, X. et al. Plant–pollinator interaction niche broadens in response to severe drought perturbations. Oecologia 197, 577–588 (2021). https://doi.org/10.1007/s00442-021-05036-0
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DOI: https://doi.org/10.1007/s00442-021-05036-0